Original Article ISSN 1984-2961 (Electronic) www.cbpv.org.br/rbpv Braz. J. Vet. Parasitol., Jaboticabal, v. 27, n. 4, p. 531-544, oct.-dec. 2018 Doi: https://doi.org/10.1590/S1984-296120180078 capilaridae in the tongue of Cerdocyon thous of free life in Brazil Nematoide capilaridae na língua de Cerdocyon thous de vida livre no Brasil Raul Henrique da Silva Pinheiro1; Isabella Bittencourt Pires Chaves2; Rogério Antonio Ribeiro Rodrigues1, Érika Branco2; Ana Rita de Lima2; Elane Guerreiro Giese1*

1 Laboratório de Histologia e Embriologia , Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, Brasil 2 Laboratório de Pesquisa Morfológica Animal, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, Brasil

Received July 18, 2018 Accepted September 05, 2018 Abstract

Studies of helminths in road-killed wild are still uncommon but may provide promising results since they can identify the parasites in juvenile and adult hosts and meet the recommendations of current discussions on bioethics that prioritize alternative methods for the use of animals. This study evaluated threeCerdocyon thous individuals that were donated after dying from being run over. Two of them had small nematode adults in the epithelial and connective tissues of the tongue. The diagnosis was based on the presence of eggs, observed in histological sections, and morphological characteristics of the in the tongue. Morphologically, this nematode has a body with transverse grooves, simple mouth opening and no lips, esophagus and stichosome with stichocytes and bacillary bands along the body, which is characteristic morphology of the family Capilariidae and genus Capillaria. The presence of this nematode in the tongue of C. thous is an extremely important fact that contributes to what is known about the biodiversity of zoonotic parasites in wild canid populations. However, an explanation for these findings remains unclear because, until now, this has not been observed in the biological cycle of the species. Keywords: Nematoda, Capillaria, mammal, Amazon.

Resumo

O estudo de helmintos de animais selvagens vitimados por atropelamento, ainda é uma prática pouco comum, porém pode ser promissor, uma vez que permite a identificação de helmintos a partir de hospedeiros juvenis e adultos, e atendem às atuais discussões em bioética, as quais priorizam métodos alternativos para o uso de animais. Foram avaliados 3 exemplares de Cerdocyon thous provenientes de doação pós-óbito por atropelamento. Dois deles apresentaram pequenos nematoides adultos inseridos nos tecidos epitelial e conjuntivo da língua. O diagnóstico foi baseado na análise de cortes histológicos que evidenciaram a presença de ovos no interior do nematoide e nas características morfológicas gerais do mesmo. Morfologicamente estes nematoides apresentavam corpo com estrias transversais, abertura bucal simples e lábios ausentes, esôfago trichuroiude com a presença de esticócitos e bandas bacilares ao longo do corpo, característica morfologicamente sugestiva da família Capillariidae e do gênero Capillaria. A presença de nematoides inseridos na língua de C. thous é um fato de extrema importância para o conhecimento da biodiversidade de parasitos zoonóticos circulantes presentes em populações selvagens de canídeos. Porém, permanece obscura a explicação para tais achados, uma vez que tal evento não foi observado no ciclo biológico das espécies até o momento. Palavras-chave: Nematoda, Capillaria, mamífero, Amazônia.

*Corresponding author: Elane Guerreiro Giese. Laboratório de Histologia e Embriologia Animal, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Av. Presidente Tancredo Neves, 2501, Terra Firme, CEP 66077-830, Belém, PA, Brasil. e-mail: [email protected]

This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 532 532/544 Pinheiro, R.H.S et al. Braz. J. Vet. Parasitol.

Introduction To extract the tongues, used in morphological studies by LaPMA, an incision in the skin and muscles of the mentonian region was Studies involving the helminthofauna of wild animals are of made. The tongue was folded ventrally after cutting the lingual great importance for the conservation of species and for public frenulum and then cut caudally at the root to harvest the material. health, since some of these parasites can injure wild populations The material was fixed in a 10% formaldehyde solution for the and have zoonotic potential (LAFFERTY, 1997). histological analysis and in an AFA solution (93 parts 70% ethyl Some helminths that parasitize wild mammals belong to the alcohol, 5 parts formaldehyde, and 2 parts glacial acetic acid) for the family Capillaridae. The taxonomy of this family is still being morphological analysis. Samples of the nematodes were separated revised and the group contains many species in the genus Capillaria from the lingual tissue, dehydrated in an ethanol series, clarified (GUARDONE et al., 2013; FUEHRER, 2014), of which with lactophenol, placed on a microscope slide under a coverslip Capillaria hepatica Bancroft, 1893 is the most commonly cited as a temporary mount, observed using a light microscope, and in the literature as a parasite of various domestic and wild animals photographed with a LEICA DM2500 microscope with an image (FREITAS & LENT, 1936; ARAÚJO, 1967; SILVEIRA et al., capturing system. This work was conducted in the Laboratório de 1975; GALVÃO, 1981; CHIEFFI et al., 1981; MANDORINO Histologia e Embriologia Animal - Instituto da Saúde e Produção & REBOUÇAS, 1991; VICENTE et al., 1997; RUAS et al., Animal. For scanning electron microscopy, fragments of the tongue 2003). Capillaria comprises a complex group of parasites, which with nematodes were fixed in 10% formaldehyde, post-fixed in has resulted in the proposal of the genera Calodium, Eucoleus, 1% osmium tetroxide, critical point dried with CO2, coated with Paracapillaria, Pearsonema and Aonchotheca (GUARDONE et al., gold-palladium and analyzed with a VEGA 3 LMU/TESCAN 2013; FUEHRER, 2014). Within this complex, three species scanning electron microscope. This was done in the Laboratório are of zoonotic importance: Paracapillaria philippinensis de Microscopia Eletrônica de Varredura - Instituto da Saúde e (Syn. Capillaria philippinensis), Eucoleus aerophila (Syn. Capillaria Produção Animal at the Universidade Federal Rural da Amazônia aerophila) and Calodium hepaticum (Syn. Capillaria hepatica, (UFRA), campus Belém. To avoid confusion, only names of genera Trichocephalus hepaticus Bancroft, 1893 and Hepaticola hepatica of helminths are abbreviated and not those of hosts. Hall 1916. Due to anthropic impacts, wild animals frequently come out Results of natural habitats in search of food and suffer injuries. Roads, starting at the construction phase, impact native fauna in several Of the three animals evaluated, two had six small adult ways, producing direct and indirect effects on populations, such as nematodes in the epithelial and conjunctive tissues of the tongue mortality from being run over, loss of habitat, dispersion of exotic (Figure 1A and 2A-C). The six nematodes formed galleries within species and intensification of the presence of humans (ASCENSÃO the epithelium (Figure 1D- E and 2B) and their dispersal had a & MIRA, 2006). The study of helminths in road-killed animals multifocal character. The diagnosis was based on the presence of is still uncommon; however, studies that use this methodology eggs (FERRER & CASTELLÀ, 1996), observed in histological are promising since they can identify these parasites in adults sections, and morphological characteristics of the nematodes in the and young individuals and meet the recommendations of current tongues, which were analyzed using scanning electron microscopy discussions on bioethics that prioritize alternative methods for (body surface) and light microscopy the use of animals (RICHINI-PEREIRA et al., 2006). In Brazil, During the histological analysis of the C. thous tongues, adult among the wild carnivores, Cerdocyon thous is one of the most female nematodes were observed in transverse sections. These were commonly road-killed species (MALHEIROS, 2004; PRADA, inserted in the basal layers of stratified epithelial tissue, with eggs 2004; PINOWSKI, 2005). both inside the parasite as well as egg isolates and clusters within Based on the few studies about the presence of capillariids in galleries developed by the nematodes (Figure 1D-E). The eggs wild animals, this study describes the first record in Brazil of a were barrel shaped with two polar opercula with plugs on the Capillariidae nematode parasitizing the tongue of C. thous, in the ends, which are diagnostic characteristics of the genus Capillaria municipality of Paragominas in Pará State, in addition to collecting (Figure 1B-C). The size and the number of nematodes inserted and analyzing retrospective data on the fauna of helminths of in the tegument of the coating of the tongue did not cause C. thous in Brazil. inflammatory reactions and did not affect the morphology of the lingual papillae (Figure 1D). Materials and Methods A light microscopy analysis of a fragment of a nematode, clarified with Amman’s lactophenol, was conducted on the anterior We evaluated the tongues of three animals (C. thous) that region of the helminth because the rest of the body was strongly were donated, after being run over by the company HYDRO inserted in the tissue and it was not possible to completely remove Paragominas - bauxite mine, to the Laboratório de Pesquisa the parasite (Figure 3A-B). Morphologically, the nematodes have a Morfológica Animal (LaPMA) - Instituto da Saúde e Produção body with transverse grooves, a simple mouth opening and no lips, Animal at the Universidade Federal Rural da Amazônia (UFRA), stichosome esophagus formed by stichocytes and bacillary bands campus Belém (under authorization of SEMA-PA Nº 455/2009 (Figure 2D) on the surface of the cuticle along the body, which and 522/2009), animals used for morphological studies. are also morphological characteristics of Capillaria (Figure 3A-B). v. 27, n. 4, oct.-dec. 2018 Capillariidae in the tongue of Cerdocyon thous 533/544 533

Figure 1. (A) Mesoscopic view of Capillaria sp. (*) inserted among the lingual filiform papillae (fi) ofCerdocyon thous in Pará State. (B) Lateral view of the Capillaria sp. female showing numerous intrauterine eggs. (C) Detail of eggs morphology with barrel shaped and two polar opercula with plugs on the ends. (D-E) Tongue photomicrographs of C. thous parasitized by Capillaria sp., in Pará State, stained with hematoxilin and eosin. (D) Lingual papillae (pl), sustained to loose connective tissue (tcf) and covered by keratinized stratified flat epithelial tissue (tep), where the Capillaria sp. (arrowhead) are inserted in interstitial space (*). (E) Cut of Capillaria sp. in keratinized stratified flat epithelial tissue (tep), sustained to loose connective tissue (tcf). Detail of cut of the nematode evidencing the cuticle (ct), uterine wall (uw), intrauterine eggs (ie), oesophagus (oe) and eggs (e) in the intertitial space (*). Scale bars: A= 1.5 cm, B=50 µm, C=20 µm, D= 200 µm, E=100 µm.

Discussion morphological characteristics of the eggs (when possible) and/or measurements of the parasite; due to the lack of data, these were In studies of the nematofauna of C. thous, published between classified only as phylum Nematoda (Table 2). 1915 and 2017, adult and juvenile nematodes in 13 superfamilies The nematodes found in the tongue ofCerdocyon thous, (Ancylostomatoidea, Ascaridoidea, Dioctophymatoidea, Filarioidea, collected in the municipality of Paragominas, Pará State, in eastern Metastrongyloidea, Oxyuroidea, Physalopteroidea, Rictularoidea, Amazon, have similar characteristics to those of other species Rhabditoidea, Strongyloidea, , Thichinelloidea, of the family Capillaridae Railliet, 1915, and genus Capillaria Trichostrongloidea) were recorded in 13 localities in Brazil Zeder, 1800. The diagnosis of infection by Capillaria in this (Table 1). Of these, 15 families, 18 genera and 24 species of study is based on the presence of eggs with bipolar plugs, as well nematodes were identified. Some taxa were not identified to the as the morphological characteristics of the nematodes found in specific level because the authors only conducted coprological the tongue. Capillariidae, one of the five families belonging to the exams. In the cases described as morphotypes, the authors provided superfamily Trichinellidea, comprise more than 300 known species 534 534/544 Pinheiro, R.H.S et al. Braz. J. Vet. Parasitol.

Figure 2. Scanning electron microscopy of Capillaria sp. parasitizing the tongue of C. thous in Pará State. (A) Overview of the parasite inserted between the lingual papillae. (B) Detail of Capillaria sp. inserted in the interstitial space formed by keratinized, stratified, flat epithelial tissue. (C) Detail of the posterior region of the nematode strongly inserted in the keratinized, stratified, flat epithelial tissue of the tongue. (D) Detail of the bacillary bands present along the body of the nematode. Scale bars: A= 100 µm, B= 10 µm, C= 50 µm, D= 5 µm.

Figure 3. Photomicrographs of Capillaria sp. parasitizing the tongue of C. thous in Pará State. (A) Overview off anterior region in lateral position, simple oral opening with no lips and initial portion of stichosome esophagus (esf); (B) Lateral view of the middle region of Capillaria sp. showing the presence of stichocytes (st). Scale bars: A= 50 µm, B= 50 µm. v. 27, n. 4, oct.-dec. 2018 Capillariidae in the tongue of Cerdocyon thous 535/544 535 e , e , c c c , e , c , b,c , Pinto et al. (2011) , Pinto et al. , Lima (2009) e e b e e , Vieira et al. , Vieira et al. (2008) b , Moraes (2016) , Moraes e e a,b They present zoonotic potential. They present b , d c c b,c b,c , Duarte (2007) , Duarte c , Pinto et al. (2011) , Pinto et al. , c b c References , Santos (2013) , Santos b , Santos (2013) , Santos (2013) , Santos , Pinto et al. (2011) , Pinto et al. , Lima (2009) b b , Moraes (2016) , Moraes , Lima et al. (2013), e e e e , Santos et al. (2015) , Santos et al. , Brandão et al. (2009) , Brandão et al. b , Santos (2008a), , Santos b,c b , Santos et al. (2015) , Santos et al. , Moraes (2016) , Moraes b,c , Curi et al. (2010) , Curi et al. c a,b Travassos (1915), Vicente et al. (1997) Vicente et al. (1915), Travassos (1943) & Freitas Travassos (2008) Vieira et al. (2002), Noronha et al. (2008) Vieira et al. Pinto et al. (2011) Pinto et al. (2003), Santos et al. (2007) (2004), Griese Santos et al. (2008) Vieira et al. (2016) (2015), Moraes Lima et al. (2013), Gomes et al. (2005) (2004), Ruas Noronha et al. (2008) Vieira et al. (2008), Ruas et al. (2007) Griese (2010) Curi et al. (2007) Brandão (2008b) (1943), Santos & Freitas Travassos (2012) Santos et al. (2011) Pinto et al. (2013) Santos (2009) Brandão et al. (2011) (2009), Pinto et al. Ribeiro et al. Gomes et al. (2015), Santos et al. (2015) (2015), Santos et al. Gomes et al. (2008) Vieira et al. (2002), Noronha et al. (2005) Curi (2012) Santos et al. (2007) Brandão Data obtained by monographs, dissertations obtained by and theses; Data c Location a SP RJ MS, RJ MS MS PE, SP, PE, MG, MS, PB ES, RS RJ, MS, PA, SP, SP PB PR, MG, PI PB, MS, RJ, PE, MG RN, CE, PI, PR, MS, PB PB, RJ, PE, RN, CE, PI PR, MG PB, PE, RN, CE, PI - - - - Data obtained by coprological examination; coprological obtained by Data b Site in host Site Instestine lung, pulmonaryHeart, artery Kidney the skin Under Kidney Small intestine, lung, Small heart and stomach intestine and stomach Small intestine Small lung, pulmonaryHeart, artery intestine Small small intestine Intestine, d distribuition in Brazilian territory according to register made for diferentes researchers between 1915 and 2017. between researchers made for diferentes territory to register distribuition in Brazilian according d d Parasite species Parasite d d Cerdocyon thous Cerdocyon Faria, 1910 Faria, (Ercolani, 1859) (Ercolani, Le Roux & Biocca, 1957 & Biocca, Le Roux (Goeze, 1782) (Goeze, Travassos, 1915 Travassos, Railliet & Henry, 1911 Railliet & Henry, d d (Werner, 1782) (Werner, (Schrank, 1788) d sp. sp. sp. Family sp. sp. Nematodes parasites of Nematodes Uncinaria carinii Uncinaria Dioctophma renale Indeterminate Dirofilaria repens Dirofilaria Ancylostoma buckleyi Ancylostoma caninum Ancylostoma braziliense Ancylostoma Ancylostoma 1 Morphotype 2 Morphotype Indeterminate 2 Morphotype 3 Morphotype 4 Morphotype Indeterminate Ascaridia galli canis Toxocara Toxocara 1 Morphotype Abbreviations of States: Ceará – CE; Distrito Federal – DF; Espírito Santo – ES; Goiás – GO; Mato Grosso do Sul – MS; Minas Gerais – MG; Pará – PA; Paraíba – PB; Paraná – PR; Pernambuco – PE; Piauí – PI; Rio de Rio – PI; Piauí – PE; – PR; Pernambuco – PB; Paraná Paraíba – PA; – MG; Pará Gerais – MS; Minas do Sul Grosso – GO; Mato – ES; Goiás Santo – DF; Espírito Federal Ceará – CE; Distrito of States: Abbreviations Review article Review of mammalian parasites in Brazil. Superfamily Ancylostomatoidea Chabaud, 1965 Superfamily Ancylostomatidae (Looss, 1905) Family 1858) (Weinland, Filarioidea Superfamily 1911) (Leiper, Onchocercidae Family a – SP; Paulo – RS; São do Sul – RN; Rio Grande do Norte – RJ; Rio Grande Janeiro e Superfamily Dioctophymatoidea Railliet, 1916 Dioctophymatoidea Superfamily (Railliet, 1915) Dioctophymatidae Family Superfamily Ascaridoidea Railliet & Henry, 1915 Ascaridoidea RaillietSuperfamily & Henry, 1853 Ascarididae Baird, Family Table 1. Table 536 536/544 Pinheiro, R.H.S et al. Braz. J. Vet. Parasitol. b c , - b c , Fer c , e , Santos et al. (2012) , Santos et al. , Vieira , Vieira (2011) e e , , c b e , Brandão (2007) , Brandão e They present zoonotic potential. They present d , Moraes (2016) , Moraes c , , e c c b,c , Ruas et al. (2008), , Ruas et al. c References , Pinto et al. (2011) , Pinto et al. b , Vieira et al. , Vieira et al. (2008) e , Vieira , Vieira (2011) (2011) , Pinto et al. , Lima (2009) , Lima (2009) , Lima et al. (2013), Moraes (2016) , Lima et al. (2013), Moraes (2010), Lima et al. (2013) , Curi et al. (2012) , Santos et al. e e e e e e e b , Vieira et al. , Vieira et al. (2008) , Ruas (2005) , Ruas b,c , Duarte et al. (2007), , Duarte et al. c b,c c , Pinto et al. (2011) , Pinto et al. b,c c Santos (2013) Santos (2008) Vieira et al. (2011) Pinto et al. (2008b) Santos (2005) (1943), Ruas & Freitas Travassos (2013) (2008), Santos Ruas et al. (2008) Vieira et al. (2011) Pinto et al. Chame (1988) (2017) Snak et al. Moraes (2016) Moraes (1971) (1927), Grisi Travassos et al. (1997) Vicente et al. (2007) Duarte (2007) Griese (2017) reira et al. (1997) Vicente et al. (1943), & Freitas Travassos (2008) Vieira et al. (2008) Vieira et al. (2009) Brandão et al. (2011) Pinto et al. Data obtained by monographs, dissertations obtained by and theses; Data c Location PE, PB, PE, RN, CE, PI PR, PB MG, MS, PI PB, RN, MS, RJ, RS, PE, CE, PI MS, PB RS, PR PI, PR RJ, GO DF MG, SP, MS, RJ MS - - Data obtained by coprological examination; coprological obtained by Data b Site in host Site Small intestine Small pulmo right ventricle, Lung, nary arteries, heart heart,Lung, small intestine, and stomach lung, pulmonaryHeart, artery Heart Stomach Stomach lung, pulmonaryHeart, artery, stomach, Cecum, large intestine Large intestine d Parasite species Parasite Linstow, 1889 Linstow, (Railliet, 1866) Linnaeus, 1758 Molin, 1860 Molin, (Travassos, 1927) Grisi, 1971 1927) Grisi, (Travassos, Scheneider, 1866 Scheneider, sp. (Froelich, 1789) (Froelich, sp. d sp. Family sp. sp. Continued... Enterobius vermicularis Enterobius 1 Morphotype 2 Morphotype 3 Morphotype 4 Morphotype 5 Morphotype praeputialis Physaloptera terdentata Physaloptera digitata Physaloptera Physaloptera Indeterminate vulpis Trichuris Trichuris Angiostrongylus railliet Angiostrongylus vasorum Angiostrongylus Aelurostrongylus Abbreviations of States: Ceará – CE; Distrito Federal – DF; Espírito Santo – ES; Goiás – GO; Mato Grosso do Sul – MS; Minas Gerais – MG; Pará – PA; Paraíba – PB; Paraná – PR; Pernambuco – PE; Piauí – PI; Rio de Rio – PI; Piauí – PE; – PR; Pernambuco – PB; Paraná Paraíba – PA; – MG; Pará Gerais – MS; Minas do Sul Grosso – GO; Mato – ES; Goiás Santo – DF; Espírito Federal Ceará – CE; Distrito of States: Abbreviations Review article Review of mammalian parasites in Brazil. Family Oxyuridae Cobbold, 1864 Family (Railliet, 1893) Physalopteridae Family Railliet, 1916 Trichinelloidea Superfamily (Ransom, 1911) Trichuridae Family a – SP; Paulo – RS; São do Sul – RN; Rio Grande do Norte – RJ; Rio Grande Janeiro Superfamily Metastrongyloidea Lane, 1917 Metastrongyloidea Superfamily 1934) (Boerhm & Gebauer, Angiostrongylidae Family Indeterminate 1926 Leiper, Protostrongylidae Family Cobbold, 1864 Oxyuroidea Superfamily 1949 Sobolev, Physalopteroidea Superfamily e Table 1. Table v. 27, n. 4, oct.-dec. 2018 Capillariidae in the tongue of Cerdocyon thous 537/544 537 e , e , e e , Pinto et al. (2011) , Pinto et al. e They present zoonotic potential. They present b d b,c b , c , Lima et al. (2013) c References , Santos (2013) , Santos Pinto et al. (2011) Pinto et al. , (2011) , Pinto et al. b e e b , Lima (2009) c , Curi et al. (2010) , Curi et al. , Santos et al. (2012) , Santos et al. b,c b,c b,c c c , Lima et al. (2013) (2011) (2010), Pinto et al. , Hoppe et al. , Ruas et al. (2008), , Ruas et al. (2008), , Ruas et al. c c c c Travassos & Freitas (1943), Santos (2008a) (1943), Santos & Freitas Travassos (2005) (2003), Ruas Ruas et al. (2008) Vieira et al. (2008) , Ruas et al. (2005) Ruas (2017) (2010), Snak et al. Curi et al. (2008) Vieira et al. Lima (2009) (2005) Ruas (2008) Vieira et al. (2013) Santos (2007) Griese (2007) Duarte Lima (2009) (2015) Lima et al. (2013), Gomes et al. (2013) Santos (2017) Snak et al. (2012) Santos et al. (2010) Curi et al. Santos (2013) Santos (2011) Vieira Data obtained by monographs, dissertations obtained by and theses; Data c Location MS, RJ, PI, MG MS, RJ, PI, RS RS, PR, MG RJ PB MG, RS, RJ PB, RN, PE, CE, PI MG, SP PB PB, MS PB, PE, RN, CE, PI PR PB, RN, CE, PI MG, PE, MG PE, PB, PE, RN, CE, PI - - - - Data obtained by coprological examination; coprological obtained by Data b Site in host Site Small intestine Small Heart, lung, pulmonaryHeart, artery Liver bladder Urinary bladder Urinary intestine, Small large intestine Intestine Small Intestine Small intestine Small (Jagerskiöld, d Parasite species Parasite d affinis pluripectinata ) ) (Bavay, 1876) (Bavay, (Diesing, 1851) (Diesing, (Bancroft 1893) (Bancroft Multipectines Multipectines ( ( (Freitas & Lent, 1935) (Freitas (Rudolphi, 1809) (Rudolphi, d sp. sp. sp. sp. sp. Family Continued... Morphotype 2 Morphotype 3 Morphotype 4 Morphotype Indeterminate hepatica Capillaria Capillaria linsi Pearsonema feliscati Pearsonema Strongyloides stercoralis Strongyloides Indeterminate Rictularia Pterygodermatites 1969 1904) Quentin, Pterygodermatites 2010 & Nascimento, Tebaldi Lima, Hoppe, Indeterminate Indeterminate lupi Spirocerca Morphotype 1 Morphotype Abbreviations of States: Ceará – CE; Distrito Federal – DF; Espírito Santo – ES; Goiás – GO; Mato Grosso do Sul – MS; Minas Gerais – MG; Pará – PA; Paraíba – PB; Paraná – PR; Pernambuco – PE; Piauí – PI; Rio de Rio – PI; Piauí – PE; – PR; Pernambuco – PB; Paraná Paraíba – PA; – MG; Pará Gerais – MS; Minas do Sul Grosso – GO; Mato – ES; Goiás Santo – DF; Espírito Federal Ceará – CE; Distrito of States: Abbreviations Review article Review of mammalian parasites in Brazil. Family Capillariidae Family Rhabditoidea Superfamily 1920 Travasso, 1934 Chitwood & McIntosh, Strongyloididae Family Rictulariidae Railliet, 1916 Family 1853 Baird, Strongylidae Family 1885 Oerley, Spiruroidea Superfamily 1932 Wehr, Chitwood & Spirocercidae Family a – SP; Paulo – RS; São do Sul – RN; Rio Grande do Norte – RJ; Rio Grande Janeiro Superfamily Rictularoidea Railliet, 1916 Rictularoidea Superfamily 1858 Weinland, Strongyloidea Superfamily e Table 1. Table 538 538/544 Pinheiro, R.H.S et al. Braz. J. Vet. Parasitol. f b,c They present zoonotic potential. They present d References , Santos (2013) , Santos b b,c , Ruas et al. (2008), Pinto et al. (2011) (2008), Pinto et al. , Ruas et al. c c Ruas (2005) Ruas Lima (2009) Lima et al. (2013) (2009) Brandão et al. Santos (2008a) Santos (2013) Santos Data obtained by monographs, dissertations obtained by and theses; Data c Location RS PB PB, PE, RN, CE, PI PI PB, PE, RN, CE, PI - - - Data obtained by coprological examination; coprological obtained by Data b Site in host Site Small Intestine Small Intestine Small Stomach Intestine, Small Parasite species Parasite Cameron. 1923 Cameron. (Travassos, 1921) (Travassos, Family sp. Continued... Morphotype 2 Morphotype felineus Molineus elegans Molineus Molineus Indeterminate 1 Morphotype 2 Morphotype 3 Morphotype 4 Morphotype 5 Morphotype 6 Morphotype 7 Morphotype 8 Morphotype Ideterminado Indeterminate 1 Morphotype Abbreviations of States: Ceará – CE; Distrito Federal – DF; Espírito Santo – ES; Goiás – GO; Mato Grosso do Sul – MS; Minas Gerais – MG; Pará – PA; Paraíba – PB; Paraná – PR; Pernambuco – PE; Piauí – PI; Rio de Rio – PI; Piauí – PE; – PR; Pernambuco – PB; Paraná Paraíba – PA; – MG; Pará Gerais – MS; Minas do Sul Grosso – GO; Mato – ES; Goiás Santo – DF; Espírito Federal Ceará – CE; Distrito of States: Abbreviations Review article Review of mammalian parasites in Brazil. Superfamily Trichostrongyloidea Cram, 1927 Cram, Trichostrongyloidea Superfamily & Schulz, 1937 Skrjabin Molineidae Family 1808) (Rudolphi, Nematoda Phylum a – SP; Paulo – RS; São do Sul – RN; Rio Grande do Norte – RJ; Rio Grande Janeiro e Table 1. Table v. 27, n. 4, oct.-dec. 2018 Capillariidae in the tongue of Cerdocyon thous 539/544 539

Table 2. Morphological description of egg morphotypes found in Cerdocyon thous, in Brazil, according to different studies conducted between 1915 and 2017. Parasite species Morphological characteristics Measurement (µm) References Superfamily Ancylostomatoidea Chabaud, 1965 Family Ancylostomatidae (Looss, 1905) Ancylostoma buckleyi Not reported 108 × 83 Santos et al. (2003) Morphotype 1 Oval shape, shell double, thin and smooth, poles big and 56.5 × 38.5 Brandão (2007), round Brandão et al. Morphotype 2 Elliptical shape, shell smooth, poles uneven 59 × 39 (2009) Morphotype 3 Elliptical or round shape, shell single, thin, smooth and 58.5 × 40 Santos (2013) transparent, embryo morulate or larvae well developed Indeterminate Not reported 54 ×33 Santos (2008b) Ascaridoidea Railliet & Henry, 1915 Ascarididae Baird, 1853 Toxocara sp. Not reported 71 × 42.5 Santos (2008b) Round shape, shell thick and covered by a rugged and ornate 85 × 76 Santos (2013) outer shell, embryonic mass in development or larvae well developed Morphotype 1 Not reported 31 × 20 Santos (2008a) Morphotype 2 Not reported 46 × 28 Morphotype 3 Elliptical shape, shell rough 61 × 36 Brandão (2007), Morphotype 4 Oval or round shape, shell double and irregularly thick 65 × 7 Brandão et al. (2009) Morphotype 5 Elliptical shape, shell thick and smooth, embryonic mass in 67 × 46 Santos (2013) development Superfamily Trichinelloidea Railliet, 1916 Family Trichuridae (Ransom, 1911) Trichuris sp. Not reported 57 × 27 Chame (1988) Not reported 57 × 25 Santos (2008a) Indeterminate Not reported 59 × 31 Indeterminate Not reported 64 ×28.6 Santos (2008b) Morphotype 1 Barrel shape, two polar opercula slightly flattened, shell thin, 55 × 25 Santos (2013) smooth and brown, embryonic mass in development Morphotype 2 Barrel shape, two opercula unequal and little prominent, 82.5 × 37.5 shell thin and clear, embryonic mass, large compared to the rest of this family Morphotype 3 Barrel shape, two polar opercula symmetric, shell thick, dark 80 × 38 brown, embryonic mass or larvae well developed Morphotype 4 Barrel shape, two polar opercula symmetric and prominent, 58 × 28 light brown, shell thick and smooth, embryonic mass in development Family Capillariidae Capillaria hepatica - 59 × 31 Ruas et al. (2003) Superfamily Physalopteroidea Sobolev, 1949 Family Physalopteridae (Railliet, 1893) Physaloptera tendernata Ellipsoidal shape, shell thin 27 × 16 Lima (2009) Physaloptera praeputialis Ellipsoidal shape, shell thin - In utero 27 × 23 Physaloptera sp. Not reported 36 × 28 Santos (2008b) Elliptical to round shape, shell thick and smooth, containing 43 × 25 Brandão et al. larvae (2009) Indeterminate Not reported 51 × 30 Santos (2008a) Indeterminate Elliptical shape, shell single, thick and smooth, larvae well 57 × 35 Santos (2013) formed Superfamily Rhabditoidea Travassos, 1920 Family Strongyloididae Chitwood & McIntosh, 1934 Indeterminate Elliptical or rounded shape, shell single, smooth, thin and 54 × 28 Santos (2013) transparent, larvae formed 540 540/544 Pinheiro, R.H.S et al. Braz. J. Vet. Parasitol.

Table 2. Continued... Parasite species Morphological characteristics Measurement (µm) References Superfamily Strongyloidea Weinland, 1858 Family Strongylidae Baird, 1853 Indeterminate Not reported Snak et al. (2017) Superfamily Spiruroidea Oerley, 1885 Family Spirocercidae Chitwood & Wehr, 1932 Not reported 25.5 × 8.5 Santos (2008b) Elliptical shape and small size, shell thick and smooth, larvae 36 × 14 Santos (2013) well developed Superfamily Trichostrongyloidea Cram, 1927 Indeterminate 40 × 18 Santos (2008a) Morfotipo 1 Elliptical shape, long and thin, shell thin and smooth, 54 × 19 Santos (2013) one side slightly convex and the other concave, larvae well developed Morfotipo 2 Elliptical shape and larger, shell thin, transparent and 65 × 29 smooth, larvae well developed Family Molineidae Skrjabin & Schulz, 1937 Molineus sp. Elliptical shape 42 × 16 Lima (2009) Indeterminate Not reported 60 ×25 Superfamily Rictularoidea Railliet, 1916 Family Rictulariidae Railliet, 1916 Pterygodermatites pluripectinata Dairy eggs - In utero 39 × 28.5 Lima (2009) Pterygodermatites affinis Dairy eggs - In utero 25 × 17 Indeterminate Round shape, shell smooth, simple and thick, larvae well 40 × 31 Santos (2013) formed Superfamily Oxyuroidea Cobbold, 1864 Family Oxyuridae Cobbold, 1864 Enterobius vermicularis Asymmetric shape, shell smooth, simple and transparent, 60 × 32 Santos (2013) larvae developed, poles unequal, one sharper and one more rounded Morphotype 1 Asymmetric shape, dark brown, simple and fluted mem- 87 × 48 brane, embryonic mass, sometimes with developed larvae Morphotype 2 Asymmetric shape, light brown or coppery, larvae robust 132 × 63 and well formed, apparently with two thin membranes in the shell Morphotype 3 Asymmetric shape, light brown or coppery, larvae robust, 185 × 83 very similar to morphotype 2, but slightly larger in size Morphotype 4 Asymmetric shape, light brown or yellowish, shell simple 212 × 93 and thin, larvae well developed Morphotype 5 Asymmetric shape, shell double and thin, colorless, larvae in 99 × 43 formation Phylum Nematoda (Rudolphi, 1808) Santos (2008a), Morphotype 1 Not reported 44 × 22.5 Brandão et al. Morphotype 2 Not reported 27 × 14 (2009), Santos Morphotype 3 Shell double and thick, larvae usually present, with protru- 34 × 19 (2013) sion at one end similar to an operculum Morphotype 4 Shell oval and thick, with rounded structure slightly pro- 60 × 47 truding at one end, may also be an operculum Morphotype 5 Elliptical shape, shell thick, simple and smooth, larvae well 45.5 × 26 formed Morphotype 6 Elliptical shape, shell transparent, thin and smooth, larvae 58.5 × 28 well formed Morphotype 7 Barrel shape, shell smooth and relatively thick, dark brown, 35 × 20 different polar regions, only one operculum, embryonic mass or larvae well developed Morphotype 8 Round shape, medium size, shell smooth, thin, transparent, 72 × 51 embryonic mass present v. 27, n. 4, oct.-dec. 2018 Capillariidae in the tongue of Cerdocyon thous 541/544 541

of nematodes that parasitize all classes of vertebrates around the reported the occurrence of eggs of Capillaria spp. in the filet of world (ANDERSON, 2000; GIBSON, 2012; STAPF et al., 2013). Pseudupeneus maculatus Bloch, 1793, a fish sold in the metropolitan In the last 100 years, three taxonomic inventories of parasites in region of Recife, Pernambuco state, and noted the zoonotic potential mammals were conducted, resulting in 13 superfamilies reported of the genus and the need for more hygienic and sanitary control for the nematofauna of C. thous in Brazil (VICENTE et al., 1997; of the quality of the product offered to the consumer. VIEIRA et al., 2008; PINTO et al., 2011). Among the nematodes For C. thous, Ruas et al. (2003) reported the first case of that comprise the nematofauna of C. thous, the members of the parasitism of C. hepatica in the state of Rio Grande do Sul. superfamily Ancylostomatoidea were the most representative In the state of Pará, Moreira et al. (2013) describes parasitism by in terms of number of species, such as Uncinaria carinii C. hepaticum in synanthropic rodents R. norvegicus and R. rattus. Travassos, 1915, Ancylostoma buckleyi Le Roux & Biocca, 1957, Although Moravec (1982) included C. hepatica in the genus Ancylostoma caninum Ercolani, 1859, Ancylostoma braziliense Faria, Calodium (Calodium hepaticum), this name is rarely used, and 1910, and Ancylostoma sp. In addition to nematode adults, two many authors place it in Capillaria. egg morphotypes were found, as well as individuals that were The site of infection of the capillariids reported in this study not identified to the specific taxonomic level; although, they had features of this superfamily. is possibly an erratic occurrence in the cycle of this parasite, and In Brazil, superfamily Trichinelloidea is represented by two the hosts acquired the infection due to certain habits, such as families, (Trichuridae and Capillariidae), three genera (Trichuris, licking the genitals and anus of other animals in the same pack. Capillaria, Pearsonema) and the following four species: Trichuris vulpis The life cycle of capillariids is monoxenic and the infection occurs Froelich, 1789, a parasite of the cecum of the large intestine in by ingestion of infective eggs after death (e.g., due to cannibalism host from Mato Grosso do Sul and Paraíba sates (VIEIRA et al., or predation) and decomposition of the host (FARHANG-AZAD 2008; LIMA 2009; PINTO et al., 2011; CURI et al., 2010; & SCHLITTER, 1978; KATARANOVSKI et al., 2010). LIMA et al., 2013); Pearsonema linsi Freitas & Lent, 1935 and The presence of capillariids in C. thous and other wild canids Pearsonema feliscati Diesing, 1851, parasites of the urinary bladder is possibly related to their diet, which includes wild and urban in host from Rio de Janeiro state (VIEIRA et al., 2008); and rodents, and is often influenced by habitat loss and the ease of C. hepatica, a parasite of the liver in host from Rio Grande do obtaining food close to urban centers. Ruas et al. (2003) describes Sul state (RUAS et al., 2003). In addition, Capillaria sp. occurs capillariids as parasites of the hepatic parenchyma and urinary bladder in different states of Brazil: Rio Grande do Sul (RUAS, 2005; of multiple hosts, which are most commonly found in rodents, RUAS et al., 2008), Paraná (SNAK et al., 2017) and Minas Gerais especially rats. Pedó et al. (2006) describe C. thous as a versatile (CURI et al., 2010). predator and that small rodent species are the most important food This is the first report of Capillariaa infection in the tongue item in its diet, with a 52.8% relative frequency, including at least C. thous of in Brazil, but the occurrence of capillariids in the seven species from distinct habits, such as open areas (Cavia aperea tongue of mammals has already been reported for other countries. Erxleben, 1777), semi-aquatic (Holochilus brasiliensis Desmarest, Copland (1975) reports that C. papuensis parasitizes the tongue 1819), cursorial in forest and open areas (Akodon sp.), semi-arboreal of Sus scrofa papuensis in Papua New Guinea. Scapino & Murphy (Oligoryzomys sp.), arboreal (Phyllomys dasythrix Hensel, 1872), (1978) describe the infection of the mucous membranes of the oral cavity of Procyon lotor, and suggests that the parasite is possibly semi-fossorial in forest and open areas (Oxymycterus sp.) and Capillaria procyonis. Snyder (1988, 1989) reports the occurrence peridomiciliary (Mus musculus Linnaeus, 1758). Birds, insects and of eggs of C. procyonis in the tongue of Procyon lotor; both accounts fruits, as well as consuming the most abundant food resources in were for Illinois, in the United States. Capillaria garfiai is reported each season, have also been reported (BISBAL & OJASTI, 1980; to parasitize the tongue of wild Sus scrofa in Spain (FERRER & BERTA 1987; MOTTA‑JUNIOR et al., 1994). CASTELLÀ, 1996). Löwenstein & Kutzer (1989) reported C. garfiai in wild boar Conclusions in Austria, found a prevalence of 69% based on histopathological studies, and demonstrated that parasitism by C. garfiai in the The presence of eggs and nematodes ofCapillaria sp. in the tongue of this animal produces small pathological changes in tongue of C. thous is extremely important, not only as a public health the lingual tissue, which is different from what is reported in this issue, but to the knowledge of the biodiversity of zoonotic parasites article, since the nematodes did not cause injury. present in wild populations of canids. However, an explanation of In Brazil, parasitism by capillariids includes different species of parasites and hosts, and C. hepatica is the most commonly cited why the eggs and nematodes were in the epithelial and connective in the literature as a parasite of wild animals, such as those found tissues of the tongue remains unclear since, until now, this has in Sciurus aestuans (FREITAS & LENT, 1936), Rattus norvegicus not been observed in the biological cycle of the species. Parasitism (ARAUJO, 1967; GALVÃO, 1981). Rattus rattus (CHIEFFI et al., of C. thous by capillariids in Pará state requires a more detailed 1981), dogs and cats (SILVEIRA et al., 1975), Tayassu tajacu investigation into the circumstances of this finding, in order to (MANDORINO & REBOUÇAS, 1991), Chrysocyon brachyurus obtain adults for morphological and molecular analyses that can (VICENTE et al., 1997) and Lycalopex gymnocercus (RUAS et al., elucidate the epidemiological implication of this parasitism and 2003). Eggs of C. hepatica were found in insects (SOLOMON & the potential zoonotic factor of this species, as well as to determine HANDLEY, 1971; FARHANG-AZAD, 1977). Lima et al. (2008) the wild rodents that can serve as reservoirs for the parasite. 542 542/544 Pinheiro, R.H.S et al. Braz. J. Vet. Parasitol.

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